Having played schoolboy football in Dublin for Home Farm, Dunne joined Everton as a 15-year-old schoolboy in the 1994–95 season. The next season, he started to play for Everton reserves and in early 1997, Dunne signed a 5-year professional contract. He was part of the successful 1998 FA Youth Cup squad along with Tony Hibbert and Leon Osman.

Dunne made his debut under then manager Joe Royle in 1997, at the age of seventeen. Under Walter Smith, however, he was often used out of position at right back, and was punished by Smith for two separate disciplinary incidents. Wimbledon reportedly had a bid accepted for Dunne, only for it to fall through, and Dunne stayed at Everton for another year, again usually filling in at right back.[3]

In the autumn of 2000, Dunne was signed by Manchester City for a fee of £3.5 million, rejoining his former manager Joe Royle.[4] City had signed both Dunne and Laurent Charvet as replacements for right back Richard Edghill who had suffered from a dip in form.

It was in the centre of defence where Dunne made his biggest impact on the team. Dunne had various partners in the centre of defence in his first season at the club and for a few games he played in a three-man defence with Andy Morrison and Steve Howey. His first season saw City relegated into the First Division and acquire the services of a new manager, Kevin Keegan. Manchester City made an instant return to the Premier League, finishing the 2001–02 season as First Division champions. Disciplinary problems in 2003 resulted in a club suspension, and his time at Manchester City looked to be over. However, Dunne returned to the first team following an intensive fitness programme, and within a few months gained an international recall.

A number of consistent performances resulted in Dunne receiving Manchester City's Player of the Year award for 2004–05, which he also won in the 2005–06, 2006–07 and 2007–08 seasons, becoming the first player to win City's PotY award four times. In the 2006 close season, at the age of 26, Dunne was appointed club captain, taking over from Sylvain Distin, amidst rumours of Distin leaving City.[5]

On 18 January 2007, Manchester City teammate Micah Richards said: “Ever since I’ve come to this club Richard has just been quality. I play with him week in, week out and I think he’s one of the best players I’ve played with. I’ve played with John Terry and Rio Ferdinand in the England squad but Richard is right up there with them."[6]

On 4 July 2008, Dunne signed a new four-year contract with Manchester City to keep him at the club until 2012.[7]

In August 2008, Garry Cook, chief executive of City, said "China and India are gagging for football content to watch and we’re going to tell them that City is their content. We need a superstar to get through that door. Richard Dunne doesn’t roll off the tongue in Beijing."[8]

Following the signings of Kolo Touré and Joleon Lescott, it was reported that Dunne could leave the City of Manchester Stadium with Aston Villa the most likely destination. Villa confirmed on 27 August 2009, that they had agreed a fee with Manchester City for the defender.[11] Aston Villa filed the paperwork for the deal before the close of the transfer window but the Premier League announced that the deal could not be "ratified" until 2 September 2009,[12] when the deal was completed.[13] Villa manager Martin O'Neill later stated the fee paid for Dunne was £5 million and that the player had signed a four-year deal.[14]

On 5 October 2009, Dunne scored his first goal for Villa, coincidentally against his former club Manchester City, in a 1–1 draw.[16] He was applauded by Manchester City fans for his respect in refusing to celebrate his goal.[17] He netted his second goal later that month in the team's 2–1 home victory over Chelsea. On 28 February 2010, he started for Aston Villa in their 2010 Football League Cup Final defeat to Manchester United at Wembley Stadium. He was named in the PFA Team of the Year for the 2009–10 season.

On 21 November 2010, he started and played the full 90 minutes alongside Ciaran Clark against Blackburn Rovers in a 2–0 defeat at Ewood Park. On 11 December 2010, Dunne was dropped from the team and replaced by Carlos Cuéllar. Dunne was recalled to the starting line up in the away game against Chelsea at Stamford Bridge which Villa ended up drawing 3–3. On 1 February 2011, he started and completed the full 90 minutes alongside James Collins in the Premier League game with Manchester United at Old Trafford in a 3–1 defeat.

On 18 March 2011, Dunne and Collins were fined a total of £200,000 – two weeks’ wages each – by Villa for a drunken confrontation with club staff during a team-bonding exercise.[18]

At the end of the 2010–11 season, Dunne made 35 appearances in all competitions for Villa. Ahead of the 2011–12 season, new manager Alex McLeish has said because of his aerial ability and such good awareness on the ball he will be an automatic first choice at the back. On 27 July 2011, he started and played the full 90 minutes in the 1–0 victory over Blackburn Rovers in the 2011 Premier League Asia Trophy held in Hong Kong. On 30 July 2011, he started the final with Chelsea and also completed the full 90 minutes in a 2–0 defeat.

On 12 February 2012, Dunne fractured his right clavicle in a collision with Joe Hart during a Premier League match against his former club Manchester City. He had surgery in Birmingham the following day.[19] Dunne travelled to the NFL team the Cleveland Browns in order to attain specialised medical care for his injury, who at the time were owned by then-chairman of Aston Villa, Randy Lerner.[20]

In May 2013, manager Paul Lambert announced that the Irishman was being released on a free transfer.[21]

Dunne holds the unfortunate record of the most own goals in the Premier League, scoring his tenth in a 3-2 defeat against Liverpool on 19 October 2014, in a game which saw QPR score two own goals to hand Liverpool the victory.[28]

QPR were eventually relegated that season, finishing in last place with 20 more goals conceded than any other side. Dunne made a total of 24 appearances.

On the 31st of May 2015, Dunne's contract expired and, along with five other players he was released by the club. There was considerable speculation regarding his plans after QPR and he was linked with moves to MLS, the Indian Super League and the League of Ireland.[29] None of these materialized however, and he formally announced his retirement from football in November 2015. He now lives with his wife and two children in Monte Carlo.[30]

Dunne was part of the Irish squad that played at the 2002 FIFA World Cup, but the centre-half pairing of Gary Breen and Steve Staunton (the latter of whom became team captain following the departure of Roy Keane) was favoured by Mick McCarthy, meaning Dunne did not even make an appearance as a substitute. The emergence of John O'Shea and Brian Kerr's preference for Kenny Cunningham meant that Dunne's chances with Ireland were extremely limited during their unsuccessful attempt to qualify for UEFA Euro 2004. He did score his fourth international goal in a friendly against Turkey just prior to the end of the campaign. Dunne again found himself out of favour with Kerr during the qualification campaign for the 2006 FIFA World Cup, only featuring in the final three matches which included a 1–0 defeat to France, a game that ultimately cost Ireland qualification. Another change of manager for Ireland saw Dunne's former teammate, Steve Staunton, use him during the majority of the Euro 2008 qualification campaign. Early defeats to Germany and a humiliating 5–2 loss to Cyprus, a match in which Dunne scored before giving away a penalty and being sent off,[33] ensured qualification was always beyond the Irish. Dunne only missed three of the twelve matches, due to suspension and injury rather than form.

On 6 September 2011, Dunne started and played the full 90 minutes in the goalless draw against Russia in Moscow. Dunne gave perhaps the best performance of his career, winning the man of the match award as he almost single-handedly stopped a Russian team which totally dominated midfield and created wave after wave of attacks. Former Ireland defender Paul McGrath described Dunne's heroics as the best performance from an Irish central defender he had ever witnessed, including his own performance against Italy in the 1994 FIFA World Cup.

Dunne in action for Ireland in September 2013.

On 11 October 2011, Dunne started and played the full 90 minutes in a 2–1 victory for Ireland over Armenia at the Aviva Stadium which gained them a play-off spot for UEFA Euro 2012, scoring in the 60th minute his eighth goal on his 69th international appearance for his country.[39][40] After the team qualified for UEFA Euro 2012 with an unprecedented 5–1 aggregate play-off win over their opponents Estonia, Dunne described it as "the best experience I've probably had in football".[41][42] He started in all three of Ireland's Group C matches at UEFA Euro 2012, as they were defeated 3–1 by Croatia, 4–0 by Spain, and 2–0 by Italy.

On 2 June 2013, Dunne made his return to the national team for the first time in a year as a second half substitution against Georgia in a 4–0 Irish win. Dunne made his return to the Irish team in his first competitive game for 15 months in a 1–2 loss to Sweden at the Aviva Stadium in 2014 FIFA World Cup qualifying.